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HSD2 neuron

From Wikipedia, the free encyclopedia
HSD2 neurons in the nucleus of the solitary tract (HSD2=green immunofluorescence; MR=red)

HSD2 neurons are a small group ofneurons in thebrainstem which are uniquely sensitive to themineralocorticosteroid hormonealdosterone, through expression ofHSD11B2. They are located within the caudalmedulla oblongata, in thenucleus of the solitary tract (NTS). HSD2 neurons are activated during a prolonged deficit in body sodium or fluid volume, as occurs after dietary sodium deprivation or during frank hypovolemia.[1] They are also activated by supraphysiologic stimulation of themineralocorticoid receptor.[2] They are inactivated when salt is ingested.[1] To date, HSD2 neurons have been identified and studied only in rats and mice.

Basic characteristics

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Brainstem(where HSD2 neurons are located)

The term "HSD2 neurons" is used in the scientific literature to refer to a subpopulation of neurons in the NTS which express both themineralocorticoid receptor (MR)[3] and11-beta-hydroxysteroid dehydrogenase type 2 (HSD2).[3][4] HSD2 is anenzyme that metabolizescortisol and otherglucocorticosteroids, which typically prevent aldosterone from binding to the mineralocorticoid receptor. Thispre-receptor mechanism for modifyinghormone binding is necessary for cellular sensitivity to aldosterone because, under physiologic conditions, cortisol circulates at 100-1000 times higher concentrations than aldosterone. As both cortisol and aldosterone bind the mineralocorticoid receptor with equal affinity, cortisol effectively crowds out aldosterone in cells without abundant HSD2. In cells with HSD2, however, aldosterone has increased access to the MR, such that increases and decreases in the circulating concentration of this hormone will produce a change in receptor activity. In HSD2 neurons (and all other cells that express both HSD2 and MR), aldosterone binds to MR and translocates it from the cytoplasm to the nucleus, causing transcriptional changes. Unlike aldosterone-sensitive cells in epithelial tissues (e.g. in the kidney), the physiologic effects of aldosterone-MR activation in HSD2 neurons are unknown. It has been suggested, but not proven, that aldosterone promotes the firing activity of these neurons.[5] Aldosterone is not necessary for HSD2 neuron activation because this can be evoked by sodium deprivation even in rats withoutadrenal glands,[1] which are the exclusive source of circulating aldosterone.

HSD2 neurons express the transcription factorPhox2b.[6] This means that HSD2 neurons probably release the excitatory transmitter glutamate onto their synaptic target neurons, as all Phox2b-expressing neurons in the NTS express the vesicular glutamate transporterVGlut2.[7] HSD2 neurons do not produce a wide array of other proteins that typify most other subtypes of NTS neurons, includingtyrosine hydroxylase,choline acetyltransferase,nitric oxide synthase,cholecystokinin,neurotensin,neuropeptide FF,substance P,somatostatin,inhibin-β,glucagon-like peptide-1,corticotropin-releasing hormone,dynorphin,calretinin, andcalbindin. A small number of HSD2 neurons (less than 2%) may express the neuropeptidegalanin.[3] Their lack of expression of the aforementioned markers suggests that HSD2 neurons form a unique subpopulation within the NTS. To date, there is no information available about the electrophysiologic characteristics of these neurons.

Input and output connections

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Theefferent projections (axonal output) of HSD2 neurons have been investigated to a significant degree using conventional neuroanatomicaltracers. Their primary output targets are thepre-locus coeruleus (pre-LC), the innermost portion of the external lateralparabrachial subnucleus (PBel), and the anterior, ventrolateralbed nucleus of the stria terminalis (BSTvl).[8] The next-order input and output connections of these target regions have been investigated in detail as well.[9][10][11] Additional information about the efferent projections of HSD2 neurons can be found in ref.[8]

Regarding theafferent (input) connections to HSD2 neurons, available information is less complete. Experiments with conventional tracers andimmunofluorescence staining have demonstrated peripheral viscerosensory input from thevagus nerve,[12] input from nearby neurons in the NTS and area postrema,[13][14] and descending input from the medialcentral nucleus of the amygdala (CeA)[15] andparaventricular hypothalamic nucleus (PVN).[16] It is likely that other sources of input exist, but a comprehensive study of HSD2 neuron afferent connections has not been conducted.

HSD2 neuron activity

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Animmediate-early gene,c-fos, has been used to study the activation and inactivation of HSD2 neurons extensivelyin vivo. The presence of nuclear c-Fos implies recent, elevated neuronal activity, and c-Fos disappears after neurons become quiescent. Very few HSD2 neurons exhibit any c-Fos in a normal animal. If, however, sodium is removed from the diet for several days to a week, most HSD2 neurons become c-Fos-positive.[17] Then, if salty food is eaten or a concentrated saline solution is imbibed, their c-Fos disappears.[1] Several other experimental conditions that reduceextracellular fluid volume—includingPEG-hypovolemia,diuresis, andadrenalectomy—also activate HSD2 neurons,[1] although none do so to as great an extent as simply removing sodium from the diet.[18]

Fos

All of these conditions, with the exception of adrenalectomy, cause a large elevation of circulating aldosterone. Correspondingly, repeated administration of the mineralocorticosteroid hormonedeoxycorticosterone acetate (DOCA) produces a moderate increase in HSD2 neuron activity (c-Fos) without any sodium or volume deficit.[2] However, even after adrenalectomy, HSD2 neurons become activated by sodium deprivation, proving that MR activation is not necessary for their activity. Thus, aldosterone may be sufficient, but is not necessary for their activation, meaning that these neurons integrate additional neural or hormonal input signals.

All of the aforementioned manipulations which activate HSD2 neurons also producesodium appetite in rats. If sodium-deprived rats are allowed access to salt, they imbibe a large quantity of it, and soon afterwards their HSD2 neurons are inactivated (they exhibit little or no c-Fos within 1–2 hours).[1][17] This phenomenon of salt-intake-induced inactivation also occurs after sodium appetite and HSD2 neuron activation are produced by DOCA, which does not produce any sodium or volume deficit.[2] Thus, HSD2 neuron inactivation by salt intake does not reflect simply the repletion of a physiologic deficit, and may instead reflect active inhibition triggered by salt ingestion. The exact mechanism for this inhibition remains unknown.[citation needed]

An interesting and unique feature of HSD2 neuron activity is that they are not activated by several stimuli that produce pronounced c-Fos activation in most other neurons in the NTS. These stimuli include severe dehydration induced by hypertonic saline administration,[19] salt ingestion (above), and changes in blood pressure. Thus, HSD2 neuronsare selectively activated by conditions which do not significantly affect surrounding NTS neurons,[1] and they arenot stimulated (or are actively inhibited) by conditions that do prominently activate most other NTS neurons.[17][19]

HSD2 neuron functions

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The close association between sodium deprivation and HSD2 neuron activation—and between salt ingestion and HSD2 neuroninactivation—led to the suggestion that these neurons are important for driving sodium appetite.[1] Other functional roles have been hypothesized. For discussion, see reviews in[18] and.[5] At present, however, no data exist to show whether these neurons are necessary or sufficient for any particular neurologic or physiologic function.

References

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  1. ^abcdefghGeerling, JC; Engeland, WC; Kawata, M; Loewy, AD (Jan 11, 2006)."Aldosterone target neurons in the nucleus tractus solitarius drive sodium appetite".The Journal of Neuroscience.26 (2):411–7.doi:10.1523/JNEUROSCI.3115-05.2006.PMC 6674421.PMID 16407537.
  2. ^abcGeerling, JC; Loewy, AD (Oct 18, 2006). "Aldosterone-sensitive NTS neurons are inhibited by saline ingestion during chronic mineralocorticoid treatment".Brain Research.1115 (1):54–64.doi:10.1016/j.brainres.2006.07.091.PMID 16935272.
  3. ^abcGeerling, JC; Kawata, M; Loewy, AD (Jan 20, 2006). "Aldosterone-sensitive neurons in the rat central nervous system".The Journal of Comparative Neurology.494 (3):515–27.doi:10.1002/cne.20808.PMID 16320254.
  4. ^Roland, BL; Li, KX; Funder, JW (Oct 1995). "Hybridization histochemical localization of 11 beta-hydroxysteroid dehydrogenase type 2 in rat brain".Endocrinology.136 (10):4697–700.doi:10.1210/endo.136.10.7664691.PMID 7664691.
  5. ^abGeerling, JC; Loewy, AD (Sep 2009)."Aldosterone in the brain".American Journal of Physiology. Renal Physiology.297 (3): F559–76.doi:10.1152/ajprenal.90399.2008.PMC 2739715.PMID 19261742.
  6. ^Geerling, JC; Chimenti, PC; Loewy, AD (Aug 21, 2008)."Phox2b expression in the aldosterone-sensitive HSD2 neurons of the NTS".Brain Research.1226:82–8.doi:10.1016/j.brainres.2008.05.072.PMC 2582384.PMID 18620340.
  7. ^Kang, BJ; Chang, DA; Mackay, DD; West, GH; Moreira, TS; Takakura, AC; Gwilt, JM; Guyenet, PG; Stornetta, RL (Aug 2007)."Central nervous system distribution of the transcription factor Phox2b in the adult rat".J Comp Neurol.503 (5):627–41.doi:10.1002/cne.21409.PMID 17559094.
  8. ^abGeerling, JC; Loewy, AD (Jul 10, 2006). "Aldosterone-sensitive neurons in the nucleus of the solitary tract: efferent projections".The Journal of Comparative Neurology.497 (2):223–50.doi:10.1002/cne.20993.PMID 16705681.
  9. ^Shin, JW; Geerling, JC; Loewy, AD (Dec 10, 2008)."Inputs to the ventrolateral bed nucleus of the stria terminalis".The Journal of Comparative Neurology.511 (5):628–57.doi:10.1002/cne.21870.PMC 2748802.PMID 18853414.
  10. ^Shin, JW; Geerling, JC; Stein, MK; Miller, RL; Loewy, AD (Sep 2011)."FoxP2 brainstem neurons project to sodium appetite regulatory sites".Journal of Chemical Neuroanatomy.42 (1):1–23.doi:10.1016/j.jchemneu.2011.05.003.PMC 3148274.PMID 21605659.
  11. ^Dong, HW; Petrovich, GD; Watts, AG; Swanson, LW (Aug 6, 2001). "Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain".The Journal of Comparative Neurology.436 (4):430–55.doi:10.1002/cne.1079.PMID 11447588.
  12. ^Shin, JW; Geerling, JC; Loewy, AD (Jan 16, 2009)."Vagal innervation of the aldosterone-sensitive HSD2 neurons in the NTS".Brain Research.1249:135–47.doi:10.1016/j.brainres.2008.10.058.PMC 2666048.PMID 19010311.
  13. ^Sequeira, SM; Geerling, JC; Loewy, AD (Sep 15, 2006). "Local inputs to aldosterone-sensitive neurons of the nucleus tractus solitarius".Neuroscience.141 (4):1995–2005.doi:10.1016/j.neuroscience.2006.05.059.PMID 16828976.
  14. ^Miller, RL; Stein, MK; Loewy, AD (Oct 13, 2011)."Serotonergic inputs to FoxP2 neurons of the pre-locus coeruleus and parabrachial nuclei that project to the ventral tegmental area".Neuroscience.193:229–40.doi:10.1016/j.neuroscience.2011.07.008.PMC 3185334.PMID 21784133.
  15. ^Geerling, JC; Loewy, AD (Aug 1, 2006)."Aldosterone-sensitive neurons in the nucleus of the solitary tract: bidirectional connections with the central nucleus of the amygdala".The Journal of Comparative Neurology.497 (4):646–57.doi:10.1002/cne.21019.PMC 2748794.PMID 16739197.
  16. ^Geerling, JC; Shin, JW; Chimenti, PC; Loewy, AD (May 1, 2010)."Paraventricular hypothalamic nucleus: axonal projections to the brainstem".The Journal of Comparative Neurology.518 (9):1460–99.doi:10.1002/cne.22283.PMC 2868510.PMID 20187136.
  17. ^abcGeerling, JC; Loewy, AD (Oct 1, 2007)."Sodium deprivation and salt intake activate separate neuronal subpopulations in the nucleus of the solitary tract and the parabrachial complex".The Journal of Comparative Neurology.504 (4):379–403.doi:10.1002/cne.21452.PMID 17663450.
  18. ^abGeerling, JC; Loewy, AD (Feb 2008)."Central regulation of sodium appetite".Experimental Physiology.93 (2):177–209.doi:10.1113/expphysiol.2007.039891.PMID 17981930.
  19. ^abGeerling, JC; Loewy, AD (Mar 2007). "Sodium depletion activates the aldosterone-sensitive neurons in the NTS independently of thirst".American Journal of Physiology. Regulatory, Integrative and Comparative Physiology.292 (3): R1338–48.doi:10.1152/ajpregu.00391.2006.PMID 17068161.
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